Accumulating comparative and
interdisciplinary research supports a brain
cooling function to yawning. In particular,
previous research has shown significant
decreases in both brain and skull temperature
following yawning in mammals. In a recent study
using a thermal imaging camera, significant
reductions in both the cornea and concha
temperature were observed following yawns in the
high-yawning subline of Sprague-Dawley rats.
Here, we performed a similar experiment to
investigate shifts in facial temperature
surrounding yawning in an avian species with
more typical yawning patterns: budgerigars
(Melopsittacus undulatus). In particular, we
took maximal surface temperature recordings from
the face (cere or eye) from 13 birds over a
one-hour period to track changes before and
after yawns. Similar to previous findings in
high-yawning rats, we identified significant
cooling (_0.36°C) of the face 10&endash;20
seconds following yawning in budgerigars.
Consistent with the hypothesis that yawns serve
a thermoregulatory function, facial temperatures
were slightly elevated just prior to yawning and
then decreased significantly below baseline
levels immediately thereafter. Similarly, birds
that yawned during the trials had consistently
higher facial temperatures compared to those
that did not yawn. Moreover, yawn latency and
overall yawn frequency were strongly correlated
with the highest facial temperature recorded
from each bird across trials. These results
provide convergent evidence in support of a
brain cooling function to yawning, and further
validate the use of thermal imaging to monitor
changes in skull temperature surrounding yawning
events.

Yawning or yawn-like mandibular gaping
patterns have been documented across vertebrate
classes, but it remains unknown whether the jaw
stretching of fish, amphibians and reptiles is
congruent with yawns observed in birds and
mammals. Nonetheless, the ubiquitous nature of
this reflexive behavior supports the view that
it is an evolved adaptation. Many researchers
have proposed hypotheses to explain the
functional significance of yawning, but few have
garnered empirical support. Comparatively, yawns
appear to serve a role in promoting arousal and
state change. The muscular contractions of the
jaw and accompanying deep inhalation of air that
characterize yawning produce significant changes
in intracranial circulation, and recently it was
posited that yawns function as a brain cooling
mechanism. Brain temperature of homeotherms is
determined by the rate of arterial blood flow,
the temperature of arterial blood flow, and any
metabolic heat production within the brain. In
particular, the physiological consequences of
yawning, i.e., enhanced blood flow to the skull
and direct heat exchange with the ambient air,
are predicted to alter the first two of these
variables by cooling brain temperature through
convective heat transfer. In addition, yawning
could lead to ventilation of the sinus system,
which would promote evaporative cooling of the
sinus mucosa. The increases in localized
circulation and changes in ventilation, which
are associated with yawning, are well known
mechanisms that cool brain temperature.

Since its conception, a growing number of
reports have tested and confirmed the specific
predictions derived from the brain cooling
hypothesis. In particular, a growing number of
studies have linked brain and/or body
temperature changes to yawning events and shown
that yawns can be effectively altered (i.e.,
selectively increased or decreased) through the
manipulation of ambient temperature. According
to this hypothesis, the onset of yawning should
be preceded by rising brain temperature, and
that once triggered yawns should produce a
measurable cooling effect. Using thermocoupled
temperature probes, Shoup- Knox et al. aimed to
directly capture this association among freely
moving Sprague-Dawley rats. Consistent with the
brain cooling hypothesis, yawning events in rats
were triggered during rapid increases in the
temperature of the prelimbic cortex tissue
(+.11°C), and following the execution of
this response brain temperatures dropped
precipitously down to baseline levels.
Comparable temperature shifts, monitored through
the use of an oral thermometer, have also been
documented surrounding excessive yawning attacks
in humans.

Recently, Eguibar et al. examined the extent
to which the aforementioned reductions in
intracranial temperature associated with yawning
produced cooling at the surface of the skull.
Using a high-yawning subline of Sprague-Dawley
rats, thermographic images of the eye cornea and
ear concha were captured before and after
yawning events. Consistent with the brain
cooling hypothesis, both cornea and concha
temperatures significantly decreased
(-0.32°C and -0.48°C, respectively)
during and 10 seconds following yawns. These
findings support the view that the physiological
consequences of yawns provide a widespread
cooling effect to the brain/skull, and not just
internal tissues, and validate the use of
thermal imaging to track changes in
thermoregulation surrounding such events. While
the use of high-yawning rats offered an
effective model to initially assess this
relationship, i.e., yawning frequency in
high-yawning rats (20 yawns/h) is an order of
magnitude higher than normal Sprague-Dawley rats
(2 yawns/h) as well as after pharmacologically-
and neuropeptide induced yawning, similar
studies are needed to replicate these findings
in animals with more typical yawning
patterns.

Here, we investigated skull surface
temperature changes as a function of yawning in
an avian species: budgerigars (Melopsittacus
undulatus). These birds served as an appropriate
non-mammalian model to explore this relationship
because much is known about their naturalistic
and experimentally-induced yawn frequency, and
yawning has previously been implicated in
thermoregulation in this species. Following a
similar methodology to Eguibar et al.,
thermographic images were continuously captured
at 10 second intervals to track immediate shifts
in facial temperature before and after yawns. In
addition, based on previous research showing a
strong correlation between body temperature and
yawning following stress within this species,
correlations were run to assess the relationship
between both yawn latency and frequency and the
maximum facial temperature measured across the
trials.

Discussion

The motor action pattern of yawning produces
profound changes in localized (i.e.,
intracranial) circulation and ventilation, which
now have well documented thermoregulatory
effects. As a follow- up to a recent report in
which decreases in skull temperature were
documented following yawns in a subline of
high-yawning Sprague-Dawley rats, we show that
yawning produces very similar reductions in the
facial temperature of an avian species with more
typical yawning patterns. In particular,
budgerigars experienced an average temperature
reduction of -0.36°C in the cere/eye region
10&endash;20 seconds after yawns, which is
consistent with the temperature decrements
detected at the eye cornea (-0.32°C) and
ear concha (-0.48°C) within the
high-yawning rats. In accord with the brain
cooling hypothesis, facial temperatures differed
considerably between birds that yawned compared
to those that did not yawn during the
experiment. Moreover, budgerigars with the
highest facial temperature recordings yawned
sooner following the onset of the recordings and
more frequently across trials. These results are
consistent with a previous study investigating
stress-induced hyperthermia in this species,
whereby a similar negative correlation was
observed between body temperature and yawn
latency. Given that the birds in the current
study were briefly handled and placed in
isolation for testing, we cannot rule out the
possibility that the yawning and associated
temperature changes reported here were also
stress-induced.

Overall, these findings suggest that yawning
is a thermoregulatory behavior in this species,
and generally support previous research
indicating a selective brain cooling function to
the opening and closing of the beak in birds
through the ventilation of the sinus system. In
budgerigars, the sinus walls contribute to
dissipation of heat through convection,
conduction and heat loss by evaporation.
Importantly, in birds the beak and surrounding
tissue is an important dissipater of heat,
because other areas are covered by plumage.
Other mechanisms used in thermoregulation around
this area include panting and gular fluttering,
which are also closely related to yawning.

In summary, the current study provides
convergent evidence supporting a widespread
brain cooling function to yawning that can be
captured through the use of thermographic images
of the skull. We suggest that future research
employ the use of thermal imaging to investigate
the relationship between yawning and
thermoregulation in other species, including
poikilotherms.